Expression interplay of calcium-binding genes and transcription factors during the osmotic phase provides insights on salt stress response mechanisms in bread wheat

Abstract

Bread wheat is an important crop for the human diet, but the increasing soil salinization is reducing the yield. The Ca2+ signaling events at the early stages of the osmotic phase of salt stress are crucial for the acclimation response of the plants through the performance of calcium-sensing proteins, which activate or repress transcription factors (TFs) that affect the expression of downstream genes. Physiological, genetic mapping, and transcriptomics studies performed with the contrasting genotypes Syn86 (synthetic, salt-susceptible) and Zentos (elite cultivar, salt-tolerant) were integrated to gain a comprehensive understanding of the salt stress response. The MACE (Massive Analysis of cDNA 3-Ends) based transcriptome analysis until 4 h after stress exposure revealed among the salt-responsive genes, the over-representation of genes coding calcium-binding proteins. The functional and structural diversity within this category was studied and linked with the expression levels during the osmotic phase in the contrasting genotypes. The non-EF-hand category from calcium-binding genes was found to be specific for the susceptibility response. On the other side, the tolerant genotype was characterized by a faster and higher up-regulation of EF-hand genes, such as RBOHD orthologs, and TF members. This study suggests that the interplay of calcium-binding genes, WRKY, and AP2/ERF TF families in signaling pathways at the start of the osmotic phase can affect the expression of downstream genes. The identification of SNPs in promoter sequences and 3-UTR regions provides insights into the molecular mechanisms controlling the differential expression of these genes through differential transcription factor binding affinity or altered mRNA stability. Key messageThe fine-tuned expression of calcium-binding genes and transcription factors during the osmotic phase underlies the susceptibility and tolerance to salt stress responses of contrasting bread wheat genotypes.